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NUTRIENT-USE EFFICIENCY AS AN INDICATOR OF STRESS EFFECTS IN FOREST TREES R. J. Luxmoore Environmental Sciences Division Oak Ridge National Laboratory Oak Ridge, Tennessee 37831-6038 ABSTRACT The ratio of plant dry weight gain to total nutrient uptake provides a lumped whole plant estimate of nutrient use efficiency (NUE), the net carbon fixed per unit of nutrient uptake. This is not a practical indicator for whole trees even if the measurement could be interpreted mechanistically. NUE is difficult to interpret since the seasonality of nutrient uptake and carbon gain may not directly coincide, and the internal supply and demand for carbon and nutrients is buffered by internal storage and matched in growth through mobilization and internal transport. Sampling of plant tissues (leaf, fine root) and solutions (phloem, xylem) for determination but provides sampling may stress effects knowledge of tree physiology and phonology. The use of nutrient use efficiency as an indicator of stress is not practical on a whole plant basis and is not definitive on a tissue basis at our present state of knowledge. of the carbon and nutrient relationships is feasible fragmented information. Frequent tissue or solution nevertheless lead to a reliable basis for interpreting on trees, but this approach requires intimate the diurnal, wetting and drying, and annual cycles of The ratio of dry weight gain to net nutrient uptake is one definition of nutrient- use efficiency (NUE). Another definition is given by the ratio of dry weight gain to nutrient content and for some tissues such as leaves, NUE is the reciprocal of nutrient concentration since leaf dry weight is the dry weight gain, and the nutrient content is the net nutrient uptake. Consideration of the utility of nutrient-use efficiency as an indicator of stress effects requires evaluation of stress effects on the relative dynamics of carbon gain and nutrient acquisition. A hyperbolic function (Fig. 1 ) describes the expected relationship between carbon gain and nutrient uptake up to the maximum carbon gain (M), where the increment in carbon gain (^C) per increment of nutrient uptake CONS is zero. The optimum carbon gain (O) is defined as the point at which the second derivative of the function is zero. In field situations, plants typically operate at about half the maximum rate of carbon gain (T). An approximately linear section of the relationship between L and the typical point (T) has one NUE value (^C//`N). Approaching the origin, NUE reaches the highest value (H); however, this condition is associated with ahnormnllv work or tivina nl~ntc' ~ lthn,, OCR for page 317
318 O R N L D W G 8 8 - 2 0 9 8 M . A o m T/ a- - H o i. ///l // ~ // ALL 1/~, !~ d NUTRIENT UPTAKE Figure 1. Relationship between carbon gain and nutrient uptake where M and O are the maximum and optimum carbon gain, TL is a linear range, and H is the highest nutrient- use efficiency. See text for discussion of a, b, c, and d. A hypothesized natural progression with increasing stand age is indicated by-- where canopy closure occurs at point T. _ uptake). If other Nutrient-use efficiency can be a useful indicator of stress if the stress causes a shift, such as Td, in the relationship (Fig. 1~. Perhaps such an effect could occur with increases in ozone exposure (reducing carbon gain) and nitrogen deposition (increasing N If other shifts in the relationship occur, such as Ta, Tb, and To, then NUE would ne a poor indicator of stress. In two cases, change in nutrient uptake or carbon gain (Ta or To, respectively) would be a better indicator of stress than NUE, whereas in the case of Tb, NUE does not change and is completely insensitive as an indicator.

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319 8 7 1 t, ~ v a, E 5 cot o ~ 4 - ._ cot - c 3 In o o s ~ 2 in 1 _ _ _ : /o~ _ / 0 o of o/ o / 8/o / l / / / / / / to/ / 0 10 20 30 40 Leat nitrogen (mg 9~' dry wt) Figure 2. Light-saturated net photosynthesis rates of leaves of Eucalyptus species with differing nitrogen concentration. Source: Reprinted with permission of Springer-Verlag N.Y., Inc. from Oecologia, 1978. Copyright 1978 by Springer-Verlag.

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320 EXAMPLES OF NUTRIENT-USE EFFICIENCY Positive relationships have been demonstrated between light-saturated net photosynthesis and foliar nitrogen concentration (Fig. 2) with occasional exceptions (Fig. 3~. In the latter case, the relationship was positive between full-sun net photosynthesis of Pintos radiata and leaf phosphorus but was negative for leaf nitrogen with the oldest needle age class generally having the lowest NUE for both nitrogen and phosphorus. Short-term phytotoxic air pollutant exposure can reduce photosynthesis (Reich and Amundson 1985), presumably reducing NUE since foliar nutrient levels change at slower rates (Sheriff et al. 1986~. Monitoring of light-saturated leaf photosynthesis and nutrient concentrations will provide valuable information on foliar functioning. In a scenario of increasing ozone exposure and nitrogen deposition, a significant shift from the nonstressed relationship between leaf photosynthesis and leaf nitrogen concentration may occur. 12 - - 1 a, - w ~ _ ~ 6 o 1 1 a I''' ~ _. , 0 0.4 0.8 1.2 0 4 8 N (g m~2) P (8 me 2) \ \ \ \ \ _ ~ b ~ . 12 16 Figure 3. Full-sun photosynthesis (Ama,,) of Pinus radiate needles in relation to leaf phosphorus (P) and leaf nitrogen (N) for current needles ----, current + 1 year , and current + 2 year ..... (from Sheriff et al. 1986~.

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321 Changes in NUE at the biochemical level are inferred for shifts to more energy- efficient nitrogen nutrition. Pate (1986) theoretically calculated the costs of nitrogen (N) assimilation in terms of adenosine triphosphate (ATP) required for various forms of N relative to ATP needed for assimilation of ammonium. Symbiotic nitrogen fixation required 16-29 mob ATP/mol NH4+, decreasing for NO3- assimilation (3-15 mol ATP/mol NH4+) with the relative energy requirements for NH4+ assimilation being 1 mol ATP in the Pate (1986) analysis. Nitrate assimilation in leaves was more efficient than root assimilation due to linkage of nitrate reduction with photosynthesis. Foliar uptake of nitric acid vapor is a more efficient N source (3 mol ATP/NH4+) than nitrate uptake into roots (15 mol ATP/NH4+~. The nitrogen-use efficiency of birch (Betula verrucosa) seedlings was shown to decrease with increase in plant nitrogen concentration in the investigations of Ingestad (1979~. Highest efficiency was obtained for the plants with lowest nitrogen concentration (Fig. 4~. The relationship between net primary productivity (NPP) of aboveground components and annual nitrogen uptake was shown by Miller ( 1984) to be linear (log-log plot) for 39 stands (r2= o.go) that included coniferous and broadleaf forests from regions that ranged from boreal to tropical (Fig. 5~. Since these data come from a wide range of natural stress conditions, it is apparent that NUE is an insensitive measure of plant response to stress. The nitrogen-use efficiency for aboveground tissues was about 170. A linear relationship was also shown between NPP and annual phosphorus uptake but with higher variability (r2= 0.74). The phosphorus-use efficiency for aboveground components was about 17. Again, this value applied to a wide range of natural stress conditions suggesting that the aboveground response of NUE to stress follows the trajectory Tb of Fig. 1. - Vitousek (1982) has suggested that for perennial vegetation, NUE is more defined in terms of the organic matter loss (or storage) per unit of (or storage). Monitoring of annual litterfall may thus provide an index of NUE. The relationship between the inverse total nitrogen in litterfall (Fig. 6) derived appropriately nutrient loss aboveground NUE. The relationship between the inverse of litter nitrogen concentration (NUE) and total nitrogen in litterfall (Fig. 6) derived for a wide range of forest communities follows the pattern of Fig. 4, in which low abscissa values are associated with high NUE. Given the rather wide scatter in the observations of Fig. 6, it may be difficult to associate any change in litter NUE with a particular stress in a monitoring program. There is much less variability if data for one species are considered, as shown by the line segments in Fig. 6 for the fertilization study of Miller et al. (1976) with Corsican pine (Pinus nigra). Determination of NUE on annual time scales restricts the identification of particular stresses with the response since many stresses impact trees during a year. Determination of NUE at shorter time steps is, however, not without problems.

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322 1 50 ~ z 100 c ' ._ ~ .~' 3 i_ _ LU ~ 50 o . . _ _ ~ Optimum~ 0 0.4 0.8 N. /0 Fresh w! Figure 4. Relationship of N-use efficiency to N status of birch (Betula verrucosa) seedlings. Nitrogen status is measured as N percentage of seedling fresh weight. The range in N status results from differing experimental N regimes (modified from Ingestad 1979~.

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323 150 100 1a 50 ~ 10 Be 0 ~ ~ I it' ~ 0 1 . 14 10 - 1a 6 s ~ 2 cam . . . . 5 10 15 30 NPP, t t)a~1 yr- / - ~ ~ ~ 0 o o o ov ~ ' . . , / ,, . 1 . . . .. 5 10 15 30 Figure S. Uptake of nitrogen and phosphorus into aboveground components as a function of net primary production (NPP) using data reported for coniferous forests from boreal ), temperate ~ ), and tropical ~ ~ regions, and for broad-leaved forests from boreal ~ ), temperate (0, Atnus rubra), and Mediterranean (~) regions. Uptake is calculated as change in accumulation over time plus release in litterfall. Both regressions are significant at P < 0.001, r2 values being 0.90 and 0.74 for N and P. respectively (from Miller 1984~.

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324 2 - 24C J tar 20C 5 0 16a o AS 2C at .. I,, 8C fir `3 4C C C C C \6C \ C C \ C C \ C Date D M _44 C ~ D T T T ~ DNT N N ~ N N T Tr T ~T_~3 ~ I I 1 1 20 ~ ~ ~ 1~ 120 140 1" 180 2= ~ IN LITTERfALL (KG HA-' YR-t ) Figure 6. The relationship between the amount of nitrogen in litterfall and the dry mass to nitrogen ratio of that litterfall. Symbols are as follows: C= coniferous, D= temperate deciduous, T= evergreen tropical, M= Mediterranean, N= temperate nitrogen fixers. The line segments link data from a long-term fertilization study by Miller et al. l 976) (from Vitousek l 982~. NUE DURING THE ANNUAL CYCLE Determination of AC/AN (NUE) during part of the growing season is a straightforward harvesting and chemical analysis exercise involving substantial effort when roots are included in a whole-plant measurement. Interpretation of the results as NUE, however, is problematic due to phenological controls on growth, utilization of internal carbon and nutrient storages, remobilization of nutrients, and the seasonality of nutrient uptake (van den Driessche l 984~. Utilization of carbon and nutrient storage in springtime foliar growth is initially "negative growth" because respiration exceeds carbon gain. Shoot growth induces nutrient remobilization from adjacent leaf and twig tissues

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325 and is essentially independent of nutrient uptake from soil (Titus and Kang 1982~; thus, NUE of shoot growth is apparently infinite. Many temperate forest species have deterministic leaf, twig, and flower growth (bud control) and indeterminant stem thickening. Root growth tends to be indeterminant but with periodic behavior due to reductions in root growth occurring during periods of shoot growth (Bevington and Castle 1985~. Due to the asynchrony of shoot and root growth, the same nutrient reserves can serve several functions during the growing season (Chapin 1980~. Fine-root (<1 mm diem) growth and mortality can be a large component of the plant-carbon budget (Santantonio and Grace 1987), and the neglect of carbon allocation to belowground processes in an aboveground determination of NUE greatly limits the interpretation of this index as a stress indicator. It is difficult to identify a time frame within the annual cycle in which measurement of AC/AN can provide an unambiguous NUE indicator of plant response to stress. Alternatively useful indicators based on carbon and nutrient dynamics may come from consideration of these components in a whole-plant physiological framework that is less constrained than the NUE concept. CARBON-NUTRIENT RELATIONSHIPS Foliar nutrient analysis (also soil chemical analysis) has been well established as a means for identifying and monitoring nutrient deficiencies in plants. Diagnostic criteria of nutrient stress (deficiency, toxicity) have been developed for a wide range of plants (Chapman 1966, van den Driessche 1974), and these can provide useful guidance, although retranslocation can mask deficiency in new foliage. Ozone exposure can result in increases in foliar nutrient concentration in some cases. Skeffington and Roberts ( 1984) showed increased Mg, K, and P concentrations in Pinus sylvestris needles exposed to 300 mg O~/m3 for 56 days but no effects from acid mist treatments. Decline in conifer growth in southwestern West Germany has been associated with Mg and Ca deficiency (Huttl and Wisniewski 1987) in needles and apparently rectified with fertilizer application. Foliar analysis will continue to be a useful indicator of plant response to stress, and the approach may be usefully extended by consideration of element ratios for elements with differing retranslocation and storage dynamics (e.g., Ca immobile, N. P. K mobile in leaves). Cotrufo ( 1985) has evaluated several tissue analysis approaches as predictors of loblolly pine response to nitrogen fertilization. Total N in xylem, total soluble N. and arginine N of twigs and needles were greater in fertilized than in unfertilized trees. Total needle N is not always a good indicator of tree N status (Ballard 1980, Sheriff et al. 1986~; however, the reliability of alternative indicators is not well established. Cotrufo ( 1985) noted that the interpretation of arginine N assays was complicated by phosphorus nutrition and soil-water status, and xylem N of loblolly pine did not show a strong relationship to N fertilization. The relationship between starch and nitrogen content has been determined in birch (Betula pendula) seedlings (McDonald et al. 1986) and in 30-year-old loblolly pine (Pinus toeda) needles (Birk and Matson 1986~; both showed a similar pattern during the growth period (Fig. 7, Fig. ~b), but the pine study conducted under field conditions showed much more variability. Variability is likely to be a problem in interpretation of carbon- nutrient relationships of tissues sampled from the field. During the dormant period (February), the pattern of starch accumulation in relation to needle nitrogen was reversed, with high starch levels being associated with high nitrogen levels (Fig. Sa).

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326 - 1 3 C] CR 250 ct 200 In Cal - Q is e go 100 is In z . 150 50 . \ - \ - 1,,.. 1 10 20 30 40 PLANT NITROGEN CONCENTRATION (me N 9 DW ) Figure 7. Steady-state dependence of plant starch concentration (ma starch g-1 dry weight) on plant nitrogen concentration (ma N g- 1 dry weight) in seedling birch (from McDonald et al. 1986).

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~- {D~ of - ~ an o c) m Z 3 - _ Cal - ~ . - 327 STARCH, mg/g 0 In 0 In 0 In 0 , . . . o 1. oo o o o pro 0 ~ o 0 0 . ' 11 11 o o o STARCH, mg/g _ ~ N U' O ~ O ~ ' ~ ~' 1l m g 0 ~, 0 _ 0 o Go o Motto , ~ ~ o o To 0 . .. . : .. Figure S. Relationship between starch and nitrogen concentrations in loblolly pine needles in control (open symbols) and fertilized (solid symbols) sites on the coastal plain of South Carolina with a 30-year old pine stand for February (a) and June (b) (from Birk and Matson 1986~. CARBON AND NUTRIENT STORAGE The principal soluble forms of nitrogen storage in woody plants are arginine, which has a high N:C ratio, and asparagine (Titus and Kang 1982) with glutamine being significant in some conifer species. Proteins are probably the most significant insoluble nitrogen reserves in trees (van den Driessche 1984~. Phospholipids and "nonhydrolyzable esters" were suggested as the main overwintering forms of phosphorus in cold-hardy species (Chapin 1980, Chapin and Kedrowski 1983~. Sulfur can be stored in proteins,

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328 amino acids, and sulfate forms (Linzon 1 97X). Potassium and inorganic phosphate accumulate in vacuoles, and calcium is probably held in exchangeable form on cell walls, particularly of xylem vessels. Starch is the dominant form of carbon storage, although secondary compounds (terpenes, latex) can be significant carbon forms in some species. Determination of the stored quantities of carbon and nutrients at the end of the growing season could become a useful indicator of plant response to cumulative environmental effects as well as of plant internal resources available for the next growing season. Titus and Kang (1982) cite several examples where high levels of storage N are highly correlated with new shoot growth of fruit trees during the following spring. Greater knowledge of how to measure internal storage and how to interpret the values for forest trees is needed before storage can be used as a definitive indicator. It is likely that not all storage locations and forms are equally accessible. Perhaps leaf starch can be more readily utilized by stem cambium than starch in ray cells of the stem. Further, the concept of capacity defined as the change in storage per unit of chemical potential energy (i.e., per unit biochemical driving force) may usefully distinguish between a range of plant storage forms. CHANGES IN CARBON-NUTRIENT RELATIONSHIPS WITH STAND AGE Nutrient retranslocation from mature leaves to new leaves (Sheriff et al. 1986), from twigs to new shoot growth, and from old roots to new roots (Titus and Kang 1982) becomes increasingly important with time as a tree increases internal nutrient storage relative to the annual growth demands. Miller ( 1984) noted that the relative demands made by forests for soil minerals decrease markedly after canopy closure; trees increasingly depend on internal retranslocation to meet nutrient requirements for annual growth. Nitrogen retranslocation in a pine plantation was calculated to increase from 11 to 69 kg ha~1 year~1 with increase in age from 10 to 40 years. Similar stand age changes were estimated for phosphorus and potassium. Meier et al. (1985) also estimated an increased contribution of retranslocation in meeting the nutritional requirements of aging Abies amabilis stands. Following canopy closure additional phytomass accumulates largely as low-nutrient wood. This implies that with increasing stand age, NUE before canopy closure is less than after canopy closure. A hypothesized progression of carbon gain in relation to nutrient uptake with increasing stand age (Fig. 1 ) would give a range of NUE values that may explain some of the variance in the data summarized by Miller In leg. 3. COMMENTS Plants tend to operate within narrow ranges in the ratios of carbon to nutrients and of nutrients to other nutrients (Chapin 1980, Garten 1976~. In the short term, plants respond to stress with a change in physiological activity per unit tissue (leaf, root); however, in the longer term, changes in leaf area and needle age classes (and, by inference, fine-root turnover) are often significant signals of plant response to stress. Continued stress, such as with high nitrogen deposition, can lead to physiological imbalances. Mohren et al. ( 1986) identified large increases in N:P ratios in Douglas fir needles in the Netherlands in recent times that were associated with phosphorus deficiency. Nambiar (1987) evaluated the ratios of calcium (generally not retranslocated) to other mobile nutrients (e.g., Ca:N, Ca:P, Ca:K) in fine-root and leaf tissues and showed the relatively greater retranslocation of mobile nutrients from senescing leaves than from old roots. It is possible that nutrient retranslocation from fine-roots may only be significant in the zone close to the root tip with the effect being masked by analysis of long lengths of root tissue. He also noted that prolonged drought had very

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329 little effect on nutrient concentrations in fine-roots. Monitoring of tissue-nutrient relationships can provide indications of stress impacts, although normal dynamics of nutrient retranslocation and storage must be understood before abnormal signals can be interpreted. SUMMARY NUE determined on annual time steps seems to be an insensitive indicator of stress since changes in carbon gain and nutrient uptake tend to occur in the same direction. Determination of NUE within a growing period is complicated by deterministic controls on growth, internal storage and retranslocation, and allocation to root processes. Light-saturated net photosynthesis generally increases with foliar nutrient (N. P) concentration, and changes in this relationship may be a sensitive indicator of short-term stress. Identification of imbalances in the relationships between carbon and nutrient dynamics of forest trees may lead to useful early warning indicators of stress impacts, but this needs to be developed within a whole-plant physiological context. ACKNOWLEDGMENT Research sponsored! by the Carbon Dioxide Research Division, U.S. Department of Energy under Contract No. DE-AC05-840R21400 with Martin Marietta Energy Systems, Inc. Publication Number 3123, Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831. REFERENCES Ballard, R. 1980. Nitrogen fertilization of established loblolly pine stands: A flexible silvicultural technique. Pp. 223-229 in Gen. Tech. Rept. S0-34, USDA Forest Service, New Orleans. Bevington~ K. B., and W. S. Castle. 1985. Annual root-growth pattern of young citrus trees in relation to shoot growth, soil temperatures, and soil-water content. J. Am. Soc. Hort. Sci. 110:840-845. Birk, E. M., and P. A. Matson. 1986. Site fertility affects seasonal carbon reserves in loblolly pine. Tree Physiol. 2:17-27. Chapin, F. S. 1980. The mineral nutrition of wild plants. Ann. Rev. Ecol. Syst. 11:233- 260. Chapin, F. S., and R. A. Kedrowski. 1983. Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous Taiga trees. Ecology 64:376-391.

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330 Chapman, H. D. (ad.). California, Riverside. 1966. Diagnostic criteria for plants and soils. University of Cotrufo, C. 1985. Progress in tissue analysis to determine the response of loblolly pine to nitrogen fertilization. Pp. 385-389 in Gen. Tech. Rept. S0-54, USDA Forest Service, New Orleans. Garten, C. T. 1976. Correlations between concentrations of elements in plants. Nature 261:686-688. Huttl, R. F., and J. Wisniewski. 1987. Fertilization as a tool to mitigate forest decline associated with nutrient deficiencies. Water Air Soil Poll. 33:265-276. Ingestad, T. 1979. Nitrogen stress in birch seedlings. II. N. K, P. Ca, and Mg nutrition. Physiol. Plant. 45: 149- 157. Linzon, S. N. 1978. Effects of airborne sulfur pollutants on plants. Pp. 109- 162 in J. O. Nriagu ted.), Sulfur in the Environment. II. Ecological Impacts. John Wiley and Sons, New York. McDonald, A. J. S., T. Lohammar, and A. Ericsson. 1986. Uptake of carbon and nitrogen at decreased nutrient availability in small birch (Betula pendula Roth.) plants. Tree Physiol. 2:61-71. Meier, C. E., C. C. Grier, and D. W. Cole. 1985. Below- and aboveground N and P use by Abies amabilis stands. Ecology 66:1928-1942. Miller, H. G. 1984. Dynamics of nutrient cycling in plantation ecosystems. Pp. 53-78 in G. D. Bowen and E. K. S. Nambiar (eds.), Nutrition of Plantation Forests. Academic Press, New York. Miller, H. G., J. M. Cooper, and J. D. Miller. 1976. Effect of nitrogen supply on nutrients in litterfall and crown leaching in a stand of Corsican pine. J. Appl. Ecol. 13:233-248. Mohren, G. M. ]., J. van den Burg, and F. W. Burger. 1986. Phosphorus deficiency induced by nitrogen input in Douglas fir in the Netherlands. Plant Soil 95:191-200. Mooney, H. A., P. J. Ferrar, and R. O. Slatyer. 1978. Photosynthetic capacity and carbon allocation patterns in diverse growth forms of Eucalyptus. Oecologia 36:103- 111. Nambiar, E. K. S. 1987. Do nutrients retranslocate from fine roots? Can. J. For. Res. 17:913-918. Pate, J. S. 1986. Economy of symbiotic nitrogen fixation. Pp. 299-325 in T. J. Givnish (ed.), On the Economy of Plant Form and Function. Cambridge University Press, New York. Reich, P. B., and R. G. Amundson. 1985. Ambient levels of ozone reduce net photosynthesis in tree and crop species. Science 230:566-570.

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331 Santantonio, D., and J. C. Grace. 1987. from biomass and decomposition data 1 7:900-908. Estimating fine-root production and turnover A compartment-flow model. Can. I. For. Res. Sheriff, D. W., E. K. S. Nambiar, and D. N. Fife. 1986. Relationships between nutrient status, carbon assimilation, and water-use efficiency in Pinus radiata (D. Don) needles. Tree Physiol. 2:73-~. Skeffington, R. A., and T. M. Roberts. 1984. The effects of ozone and acid mist on Scots pine saplings. Report TPRD/L/2695/NS4, Central Electricity Generating Board, Surrey, United Kingdom. Titus, J. S., and S. M. Kang. 1982. apple trees. Hort. Rev. 4:204-246. Nitrogen metabolism, translocation, and recycling in van den Driessche, R. 1974. Prediction of mineral nutrient status of trees by foliar analysis. Bot. Rev. 40:347-394. van den Driessche, R. 1984. Nutrient storage, retranslocation, and relationship of stress to nutrition. Pp. 181-209 in G. D. Bowen and E. K. S. Nambiar (eds.), Nutrition of Plantation Forests. Academic Press, New York. Vitousek, P. 1982. Nutrient cycling and nutrient-use efficiency. Am. Nat. 119:553-572.

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